Consequences of Intraspecific Variation in Female Body Size in

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     Consequences of Intraspecific Variation in Female Body Size in
  Stagmomantis limbata (Mantodea: Mantidae): Feeding Ecology, Male
                   Attraction, and Egg Production
                               MICHAEL R. MAXWELL1          AND   CAYLIN FRINCHABOY
          Department of Mathematics and Natural Sciences, National University, 11255 North Torrey Pines Road,
                                                 La Jolla, CA 92037

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                      Environ. Entomol. 43(1): 91Ð101 (2014); DOI:
       ABSTRACT Body size is an important feature of organisms, inßuencing many components of life
       history and Þtness, such as feeding success and reproductive output. Body size is considered especially
       salient for solitary predators, whose food intake hinges on individual predation success, which in turn
       is often driven by the relative sizes of predator and prey. The current study examined intraspeciÞc
       variation in adult female length and its Þtness consequences in a solitary predator, the praying mantid
       Stagmomantis limbata Hahn. Through a 5-yr integration of observational and experimental work in the
       Þeld and captivity, we investigated the relationship between female pronotum length and prey size,
       diet breadth, male attraction, and measures of egg production (fecundity and ootheca mass). We found
       that longer females ate longer prey in the Þeld and showed greater breadth of prey size than shorter
       females. Longer females did not necessarily feed at higher rates in the Þeld, as measured by the rate
       of abdominal expansion. Female length failed to show signiÞcant effects on male attraction or on the
       incidence of cannibalism. Longer females had higher fecundity (mature eggs in body at death) and
       laid heavier oothecae than shorter females. In nature, longer females consistently emerged as adults
       earlier in the season than shorter females. Shorter female adults emerged when feeding rates were
       higher in the Þeld, suggesting an incidental ecological beneÞt of shorter adult size.

       KEY WORDS body size, prey size, Þtness, praying mantis, Stagmomantis limbata

Body size is an important feature of organisms, as it         Solitary predators include praying mantids (Manto-
inßuences many components of life history and Þtness          dea), elongate insects that exhibit considerable inter-
(Peters 1983, Roff 1992, Stearns 1992, Hone and Ben-          speciÞc variation in body length, from 1 cm to ⬎15 cm
ton 2005). In many organisms, increasing body size            (Ehrmann 2002). Mantids have been the subject of
results in increased diet breadth, longevity, and re-         many studies on foraging theory and community ecol-
productive output, both between and within species            ogy (Charnov 1976, Holling et al. 1976, Hurd and
(Peters 1983, Andersson 1994, Chown and Gaston                Eisenberg 1990, Moran et al. 1996; reviewed in Hurd
2010). Research on predatory species typically reveals        1999, Fagan et al. 2002). Examinations of the ecolog-
that prey size and diversity increase with predator size      ical consequences of size variation in mantids have
(Schoener 1971, Wilson 1975, Cohen et al. 1993, Costa         focused primarily on interspeciÞc variation (Hurd and
2009). For prey, large body size may afford protection        Eisenberg 1989a,b; reviewed in Hurd 1999). In a metaÐ
from predation (Paine 1976, Polis 1988). Consider-            analysis of the impacts of three mantid species on the
ations of relative size between individuals are espe-         Þeld assemblages of arthropod prey, Fagan et al.
cially relevant for cannibalistic species, where the          (2002) detected different impacts for different spe-
consumer and consumed are often determined by                 cies, suggesting difference in body size as a probable
relative size (Fox 1975, Polis 1981, Claessen et al.          contributing factor. In a Þeld study of two other man-
2000). Within a species, large body size has been found       tid species, Maxwell and Eitan (1998) demonstrated
to correlate with fecundity and mating success                interspeciÞc differences in body length measure-
(Honek̆ 1993, Andersson 1994, Bonduriansky 2001).             ments, with longer species eating longer prey than the
   Body size is considered to be particularly important       shorter species.
for solitary predators, whose food intake hinges on              The Þtness consequences of intraspeciÞc variation
individual predation success, which in turn is often          in size in mantids have received relatively less atten-
driven by the relative sizes of predator and prey (Wil-       tion. A few studies have documented variation in size
son 1975, Claessen et al. 2002, McCoy et al. 2011).           in natural populations within nymphal stadia and
                                                              among adult females (Matsura et al. 1975, Hurd and
 1   Corresponding author, e-mail:           Eisenberg 1989a, Maxwell and Eitan 1998). Studies in

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92                                   ENVIRONMENTAL ENTOMOLOGY                                         Vol. 43, no. 1

captivity show that variation in body mass and length       of cannibalism (Moya-Laraño et al. 2003, Wilder and
among early instars can be generated by differences in      Rypstra 2008). To test our hypotheses, we integrated
food per capita (e.g., Hurd and Rathet 1986, Dussé and     naturalistic observations with Þeld experiments and
Hurd 1997, Moran and Hurd 1997), as suggested by            work in captivity.
Þeld manipulations of nymphal density (Hurd and
Eisenberg 1984, Fagan and Hurd 1994). The conse-
                                                                            Materials and Methods
quences of intraspeciÞc size variation have been re-
stricted to captivity. From HollingÕs morphometric             Field Observations: Biometry, Feeding Ecology,
models of mantids as predators (Holling 1964, Holling       and Behavior. We measured and observed adult fe-
et al. 1976), longer individuals can be expected to         males at a Þeld site along Baker Creek in Big Pine, CA
attack larger prey, as appears to be the case in captive    (37⬚ 10⬘ N, 118⬚ 17⬘ W) for 4 yr (2008 Ð2011). At this
studies on Tenodera aridifolia (Stoll, 1813) (Hurd          site, populations are nonoverlapping and univoltine,
1988, Iwasaki 1991, Whitman and Vincent 2008). In-          with hatching occurring in spring, adults Þrst appear-
traspeciÞc size variation can have reproductive con-        ing in August, persisting through late September, and

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sequences, as Matsura et al. (1975) suggest a positive      dying off in October with the onset of cold temper-
relationship between body length and ootheca (egg           atures. Mantids occur along the banks of the creek,
case) mass in T. angustipennis Saussure. In staged mat-     which are dominated by willow (Salix sp.), black lo-
ing trials, however, neither adult female length nor the    cust (Robinia pseudoacacia L.), rose hips (Rosa wood-
degree of mate size dimorphism was found to affect          sii Lindley), and long-leaved aster (Aster ascendens
the occurrence of female-on-male cannibalism in the         Lindley). In S. limbata, as in many mantids, the ßight-
mantids Pseudomantis albofimbriata Stål and Stagmo-         less females are somewhat sedentary, allowing for re-
mantis limbata Hahn (Barry et al. 2008, Maxwell et al.      peated measurements and observations of individuals
2010b).                                                     in nature (Maxwell 1998, Maxwell et al. 2010b).
   The current study examines the consequences of              Field observations were conducted through weekly
intraspeciÞc size variation in a Þeld setting for the       censuses in 2008 and daily monitoring of marked fe-
mantid S. limbata, which is native to North America,        males from 2009 to 2011, based on methods described
occurring from the western United States into South         by Maxwell et al. (2010b). In 2008, we conducted six
America (Roberts 1937, Ehrmann 2002). Females typ-          weekly censuses between 20 August and 27 Septem-
ically exceed 50 mm in body length and 1.5 g in body        ber. Each census covered the same 847-m section of
mass after a few weeks of feeding as adults, whereas        the creekside. To conduct each census, we visually
males rarely exceed 50 mm or 0.5 g as adults. Females       searched for S. limbata between 0900 and 1600 hours,
are ßightless, solitary ambush predators, while males       gently shaking the vegetation within 2 m of the creek
are ßight-capable and more mobile than the females.         bank. For each adult found, we recorded sex, prono-
Roberts (1937) documented variation in the number           tum length (to 0.1 mm), dorsoventral abdominal
of nymphal stadia within captive colonies, suggesting       thickness (females only, to 0.1 mm), underwing col-
intracohort variation in size among adults. In nature       oration, and any intersexual interactions (i.e., mount-
and captivity, variation in a measure of adult length,      ing of the female by the male, copulation, and canni-
pronotum length, exists between years (Maxwell and          balism). For a given stage (i.e., nymphal stadium or
Eitan 1998, Maxwell et al. 2010b). In S. limbata and        adult), pronotum length is Þxed and does not expand
other mantids, manipulations of the feeding regime          as the mantid feeds, thereby serving as a standard
within cohorts of adult females have demonstrated           index of length in mantids (e.g., Lawrence 1992, Max-
important effects on fecundity, the occurrence of in-       well 1998). We used hind wing coloration to identify
tersexual cannibalism, and male behavioral responses        newly emerged adult females, as females have diffuse
(Matsura and Morooka 1983; Birkhead et al. 1988;            yellow underwings upon adult emergence, developing
Lelito and Brown 2008; Barry et al. 2010; Maxwell et        into a tessellated pattern of distinct yellow cross veins
al. 2010a,b). The Þtness effects of variation in female     by 4 Ð 8 d postemergence (Maxwell et al. 2010b). For
length remain unknown in natural populations.               a female found with diffuse yellow underwings, we
   The current study examines variation in female           assigned the date of discovery as the femaleÕs date of
length and its consequences in a multiyear study on S.      adult emergence. Prey items being eaten by the man-
limbata. SpeciÞcally, we investigate the relationship       tids were taxonomically identiÞed and measured to 1
between adult female length and prey size, diet             cm. All adults were individually marked with perma-
breadth, male attraction, and measures of egg produc-       nent ink on the pronotum for later identiÞcation, and
tion (fecundity and ootheca mass). Based on the ex-         were released at the spot of capture. To assess feeding
isting literature, we expect longer females to eat larger   rate, we measured abdominal thickness of all resighted
prey, show greater diet breadth, and show higher            females (Maxwell et al. 2010b).
fecundity and ootheca mass. With regard to male at-            From 2009 to 2011, we conducted daily monitoring
traction, we test two competing predictions. Female         of females. In each year, we found females for obser-
length might correlate with the amount of pheromone         vations through daily searches within the 847-m sec-
produced, and longer females might be more attrac-          tion of creekside by the methods described above (i.e.,
tive because of increased fecundity (Prenter et al.         visually searching through the vegetation between
1994, Bonduriansky 2001). Alternatively, males might        0900 and 1600 hours). The 847-m section was divided
avoid longer females if such females pose a greater risk    into thirds, and one-third was searched each day such
February 2014                MAXWELL AND FRINCHABOY: INTRASPECIFIC SIZE VARIATION IN S. limbata                        93

that each third was searched every 3 d. We marked             We collected 24 recently emerged adult females from
each adult for later identiÞcation and recorded mor-          a site 300 m upstream from the 847-m study section of
phological and behavioral data, as described above. In        Baker Creek between 22 August and 8 September.
2009 and 2010, we measured the body length of each            Each female had diffuse yellow underwings, indicat-
adult upon Þrst sighting (front of head to end of             ing recent adult emergence, and was assigned as either
abdomen, to 1 mm). At the start of each daily census,         “short” (pronotum length range ⫽ 18 Ð20 mm, n ⫽ 12)
we checked the behavior of all previously marked              or “long” (pronotum length range ⫽ 22Ð24 mm, n ⫽
females (i.e., intersexual interactions and prey items).      12). Each female was maintained in a ventilated 1.6-
We measured the abdominal thickness of females                liter polyethylene container in an outdoor shelter at
12Ð16 d after Þrst sighting to minimize physical han-         the Owens Valley Laboratory (University of Califor-
dling of the females. Daily censuses and monitoring of        nia, Bishop, CA). Each female was provided one
marked females occurred in the periods 11 August to           cricket nymph (Acheta domesticus L.) every 2 d from
5 September 2009, 8 September to 15 October 2010,             capture until 15 September. Over this feeding period,
and 29 August to 29 September 2011. In 2009, we               the abdomen of each female increased to at least 9 mm

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stopped daily censuses on 6 September, but continued          in thickness, indicating a mature clutch of eggs and
to daily monitor previously marked females until 28           sexual receptivity (Maxwell et al. 2010b); mean ⫾ SE
September. As we monitored these females, we                  abdominal thickness ⫽ 10.3 ⫾ 0.2 mm (n ⫽ 24).
marked, measured, and recorded behavior of any en-               We placed the females at the Baker Creek site on 15
countered unmarked adults.                                    September at 1100 hours. Each female was placed in
   For observed predation events in the Þeld (2008 Ð          a plastic mesh cage (17 by 17 by 5 cm) that was
2011), we examined the relationship between female            overlain with four layers of light cotton gauze to re-
pronotum length and prey length through correlation.          duce visual cues and signals. In addition to the 12 short
We analyzed the effect of female pronotum length on           and 12 long females, we set out six empty covered
diet breadth by Þrst sorting the females by pronotum          cages to verify our expectation that males would not
length, and constructing two subgroups of females for         be attracted to the cages per se, based on previous
comparison: the shortest third (i.e., the shortest 33%) and   research (Maxwell et al. 2010a, 2010b). The 30 cages
the longest third (longest 33%). For each subgroup of         were placed at 20-m intervals along a 600-m contin-
females, we deÞned diet breadth as the subgroupÕs sam-        uous stretch of bank of Baker Creek, in the pattern
ple variation in observed prey length. We then compared       empty-short-long-short-long replicated sixfold. Each
diet breadth between the two subgroups through Lev-           cage was fastened to vegetation at a height 1.0 Ð1.5 m.
eneÕs test of two variances (Zar 2010).                          We checked the cages at 1000 and 1430 hours on
   To assess feeding rates of adult females in the Þeld,      each of the three consecutive days (16 Ð18 Septem-
we analyzed the rate of abdominal expansion of young          ber). We recorded any male found on a cage or within
adults in all years from 2008 to 2011 (Maxwell et al.         30 cm of the cage. All males were removed and kept
2010b). Young adult females were identiÞed as those           in isolated containers at the Owens Valley Laboratory
having diffuse yellow underwings at Þrst sighting. The        to eliminate possible effects of experience on male
rate of abdominal expansion was calculated as:                behavior. To replace these captured males, an equal
                                                              number of males collected from the Owens Valley
                 Rate ⫽ 共a 2 ⫺ a 1)/t,                 [1]
                                                              Laboratory were released 50 m orthogonal to the fe-
where a2 ⫽ dorsoventral abdominal thickness (milli-           male cage at the midpoint of the linear 600-m stretch
meters) 12Ð16 d after the Þrst sighting, a1 ⫽ dorso-          at 1600 hours on each day. The experiment was ter-
ventral abdominal thickness (millimeters) at Þrst             minated after the check at 1430 hours on 18 Septem-
sighting, and t ⫽ the actual number of days between           ber. All captured males and females were retained for
a2 and a1 measurements. This analysis was restricted to       further work in captivity. All but 10 females were
females measured within 12Ð16 d after the Þrst sight-         maintained until they died in captivity; the 10 females
ing, as this period is typically too early for a recently     were released at Baker Creek on 29 September.
emerged female to copulate and oviposit. In the cur-             Field Observations: Female and Male Pairings.
rent study, the average age of copulation was 15 d for        Through the methods described above, we observed
females in the Þeld (see Results). While the minimum          pairings in the Þeld. We deÞned a pairing as a male
age of copulation for these females was 4 d, the current      mounted on a female, or a male and female in copu-
study found that the average interval between the Þrst        lation. Within each year, we compared the pronotum
copulation and the Þrst oviposition was 12 d for well-        lengths of females observed in at least one pairing with
fed females in captivity (see Results). Thus, for the         those of all other females measured at the Þeld site.
young adult females observed in the Þeld, abdominal           These comparisons incorporate the combined effects
expansion during the Þrst 12Ð16 d was unlikely to be          of all relevant stimuli (e.g., chemical, visual, tactile) on
confounded by abdominal ßattening after oviposition.          male attraction.
   Reproduction: Male Attraction, Natural Pairings,              Female Fecundity and Ootheca Mass. We analyzed
Fecundity, and Ootheca Mass. Field Experiment: Fe-            the relationship between female pronotum length and
male Length and Male Attraction. In 2011, we con-             fecundity (number of mature eggs in body at death)
ducted a Þeld experiment to examine male response to          and ootheca mass in three generations of females
females of different pronotum lengths (long vs. short),       (2006, 2008, and 2010). In all years, we obtained virgin
with emphasis on chemical attraction by the females.          adult females through the collection and rearing of
94                                   ENVIRONMENTAL ENTOMOLOGY                                             Vol. 43, no. 1

late-instar nymphs and young adults from several Þeld
sites in Bishop and Big Pine, CA, during July through
September. Each nymph and adult was isolated in a
ventilated 1.6-liter polyethylene container. In 2006,
nymphs and adults were transported to an outdoor
shelter on a private property near National University,
La Jolla, CA (32⬚ 55⬘ N, 117⬚ 15⬘ W). In 2008 and 2010,
nymphs and adults were maintained in an outdoor
shelter at the Owens Valley Laboratory at Bishop until
28 September 2008 and 17 October 2010, respectively,
after which all adults were transported to the shelter
near National University. Each nymph was provided
with misted water and one house cricket nymph every
2 d, supplemented with mealworms (Tenebrio molitor

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L.). Mantid nymphs were checked daily for adult
emergence. Through these methods, we obtained over
70 virgin females in all years (n ⫽ 73Ð151 per year). We
measured pronotum length of all adult females. Adult
females were provided a standardized diet of one
house cricket nymph every 2 d.                                 Fig. 1. Pronotum length (millimeters) for adults mea-
   We measured fecundity in 2006 and 2008 for captive       sured in the Þeld, 2008Ð2011. White boxes indicate females;
females that did not copulate, did not lay oothecae,        black boxes indicate males. Horizontal bars indicate mean for
and did not cannibalize males. Fecundity was mea-           each sex within a year, with ⫾ SE indicated by box; whisker
sured by dissecting the females upon death and count-       lines indicate 5th and 95th percentiles. Different letters in-
                                                            dicate signiÞcant difference between groups (Tukey com-
ing mature eggs (i.e., 5Ð 6 mm in length and rich orange    parisons, family-wise ␣ ⫽ 0.05). For each group, n ⫽ 56Ð185
in coloration). We analyzed females that lived for at       adults.
least 20 d postemergence, as S. limbata undergo a
feeding period to develop a clutch of eggs (n ⫽ 18 in
2006, n ⫽ 12 in 2008).                                        For the second measure of body condition, we used
   To obtain oothecae, we paired virgin females and         the unstandardized residual values from the linear
Þeld-collected adult males in 2010 (n ⫽ 26 pairings).       regression of female body mass at mating trial on
Pronotum length of the females spanned 17Ð22 mm.            pronotum length.
To standardize recent feeding and mating history              Statistical Analyses. We performed statistical anal-
among the captured males, each male was fed one             yses on the software SPSS 17.0 (IBM Co., Chicago, IL).
cricket nymph every 3 d for a minimum of 7 d before         All inferential tests are two-tailed, and mean ⫾ SE
use in a mating trial. Mating trials consisted of random    values are reported for descriptive statistics. When
pairings of the females and males between 18 Sep-           multiple univariate tests are conducted for a particular
tember and 16 October 2010 at the Owens Valley              analysis, we lower alpha (␣) by the sequential Bon-
Laboratory. At each trial, we weighed each female           ferroni technique (Rice 1989).
(0.01 g) and measured dorsoventral abdominal thick-
ness (0.1 mm); mean ⫾ SE female age at trial ⫽ 19 ⫾
1 d. Each pair was placed in a screen cage (45 by 45
by 50 cm) and was allowed to interact for 10 h. Each           Field Observations: Pronotum Length. Mean pro-
female copulated with her paired male and did not           notum length for females was 21.0 mm (SE ⫽ 0.1, n ⫽
cannibalize him. We weighed the Þrst ootheca (0.01 g)       589, all years combined), and mean pronotum length
laid by each female for analysis.                           for males was 14.9 mm (SE ⫽ 0.047, n ⫽ 359, all years
   In the analysis of ootheca mass, we included two         combined). Females were consistently longer than
measures of female body condition: slope-adjusted           males in all years, with signiÞcant variation between
ratio and regression residuals (Petrie 1983, Jakob et al.   years within both sexes (Fig. 1; ANOVA: whole-model
1996, Moya-Laraño et al. 2008). The slope-adjusted         F7,940 ⫽ 739.7; P ⬍ 0.001, year P ⬍ 0.001, sex P ⬍ 0.001,
ratio uses the general equation:                            year ⫻ sex interaction P ⬍ 0.01).
                                                               Pronotum length accurately reßected body length,
                     m ⫽ k ⫻ l a,                    [2]    as evidenced for adults in 2009 and 2010. For females,
                                                            a strong, positive relationship was found between pro-
where m ⫽ body mass at mating trial, l ⫽ pronotum           notum length and body length measured at the Þrst
length, and k and a are scaling parameters that vary        sighting (Multiple regression: F2,232 ⫽ 212.6; adjusted
according to species (Peters 1983). For S. limbata          R2 ⫽ 0.64, whole-model P ⬍ 0.001, pronotum length
females, k ⫽ 0.13 and a ⫽ 2.63 (Maxwell 1998), yield-       P ⬍ 0.001, year P ⬎ 0.2; Pearson correlation between
ing the following equation for body condition as a          pronotum length and body length: r ⫽ 0.80, P ⬍ 0.001).
slope-adjusted ratio:                                       For both years combined, mean body length for fe-
                                                            males was 57 mm (SE ⫽ 1 mm, range ⫽ 44 Ð 69 mm, n ⫽
        Body condition ⫽ m/(0.13 ⫻ l 2.63)           [3]    235). For males, pronotum length and body length
February 2014                MAXWELL AND FRINCHABOY: INTRASPECIFIC SIZE VARIATION IN S. limbata                               95

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  Fig. 2. Pronotum length (millimeters) for newly emerged adult females in the Þeld. Date of adult emergence is on x-axis;
numerical dates are Julian dates, where 1 August ⫽ 213. (a) 2008, n ⫽ 27 females. (b) 2009, n ⫽ 37 females. (c) 2010, n ⫽
20 females. (d) 2011, n ⫽ 29 females.

were similarly related (Multiple regression: F2,112 ⫽            Average prey lengths for each year are given in Fig.
155.1; adjusted R2 ⫽ 0.73; whole-model P ⬍ 0.001,             3a. For years with at least 10 predation events (i.e.,
pronotum length P ⬍ 0.001, year P ⬎ 0.7; Pearson              2009, 2010, and 2011), nonmale prey length failed to
correlation: r ⫽ 0.86, P ⬍ 0.001). For both years com-        differ signiÞcantly among years (Kruskal-Wallis test
bined, mean body length for males was 46 mm (SE ⫽             with tied ranks: Hc ⫽ 2.89; df ⫽ 2; P ⬎ 0.2). The
1 mm; range ⫽ 39 Ð55 mm; n ⫽ 115).                            inclusion of conspeciÞc males increased the mean
   For newly emerged adult females in the Þeld, a             prey length for 2011 (Fig. 3a), causing this year to
negative relationship between pronotum length and
inferred emergence date was evident in all years (Fig.            Table 1. Predation events by adult female S. limbata in the
2). A negative correlation was signiÞcant in all years,       field, 2008 –2011
with r ⬍ ⫺0.5, P ⬍ 0.01 in all years (range of Pearson
correlations ⫽ ⫺0.76 to ⫺0.55).                                                                                 Prey
                                                               Prey taxon (Order: Family: Genus and species)   length
   Field Observations: Feeding Ecology. We observed                                                             (cm)
73 females with prey items in the Þeld (Table 1). Ten
prey items were conspeciÞc males, which involve the           Diptera (misc. ßies)                               1           9
                                                              Hymenoptera: Apidae: Apis mellifera                1          33
possible confounding inßuence of sexual attraction on           (honeybee)
predation success. Females that were observed to can-         Hymenoptera: Vespidae (unidentiÞed yellow          1           3
nibalize males did not signiÞcantly differ in pronotum          jackets)
length from females that were not observed to can-            Hymenoptera: Vespidae: Polistes sp. (paper         2           2
nibalize males (mean ⫾ SE: 21.3 ⫾ 0.4 mm, n ⫽ 10              Hymenoptera (unidentiÞed wasp)                     1           1
cannibalistic females; 20.9 ⫾ 0.2 mm, n ⫽ 63 noncan-          Lepidoptera (unidentiÞed butterßy)                 2           1
nibalistic females; t-test: t71 ⫽ 0.8, P ⬎ 0.4). Three prey   Mantodea: Mantidae: Stagmomantis limbata           6           3
items were conspeciÞc females. In two of these cases,           female
                                                              Mantodea: Mantidae: Stagmomantis limbata           5          10
the femalesÕ pronotum lengths were known, and the               male
consumed females had shorter pronota than the con-            Orthoptera: Acrididae: Melanoplus femurrubrum    2Ð3a         10
sumer females. For the 63 nonmale prey items, the               (red-legged grasshopper)
majority (46 events, or 73%) were 1 cm in length,             Orthoptera: Tettigoniidae (unidentiÞed             3           1
making assumptions regarding normality of data dif-
Þcult to evaluate. Thus, we used nonparametric sta-             All prey items are insects.
tistical tests on prey length data.                             a
                                                                  Two prey lengths observed: 2 cm (n ⫽ 1), 3 cm (n ⫽ 9).
96                                    ENVIRONMENTAL ENTOMOLOGY                                           Vol. 43, no. 1

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   Fig. 3. Predation events by adult females in the Þeld, 2008Ð2011. (a) Prey length (centimeters) by year. Sample sizes
are given in parentheses; the Þrst number represents all prey, except conspeciÞc males; the second number is the number
of conspeciÞc males. Black diamonds: mean (⫾SE) prey length, excluding conspeciÞc males. White diamonds: mean (⫾SE)
prey length, including conspeciÞc males. (b) Female pronotum length (millimeters) and prey length (centimeters). White
squares: conspeciÞc males (n ⫽ 10); black diamonds: all other prey (n ⫽ 63). Vertical dashed lines divide the 63 nonmale
predation events into thirds, sorted by female pronotum length.

differ from the other 2 yr (Kruskal-Wallis test with tied       To examine the effect of female pronotum length on
ranks: Hc ⫽ 14.32; df ⫽ 2; P ⬍ 0.001).                       diet breadth, we examined the sample variations in
   For all years combined, adult female pronotum             prey length for the shortest-third and longest-third
length and observed prey length were positively cor-         females (indicated in Fig. 3b). The shortest-third fe-
related for nonmale prey (Fig. 3b; Spearman correla-         males ate shorter prey than the longest-third females
tion: rs ⫽ 0.38; P ⬍ 0.01; n ⫽ 63). This correlation was     (mean prey length ⫽ 1.1 cm and 2.1 cm, respectively;
maintained when cannibalized males were included in          Mann-Whitney test: U ⫽ 305; n1 ⫽ n2 ⫽ 21; P ⬍ 0.01).
analysis (Spearman correlation: rs ⫽ 0.34; P ⬍ 0.01; n ⫽     The shortest-third females showed a narrower
73). Given the negative correlation between adult            breadth in prey length than the longest-third females,
emergence date and pronotum length, we checked for           evinced by smaller variance (0.2 vs. 2.5 cm2, respec-
a possible inßuence of the date of predation on prey         tively; LeveneÕs test, normality of data not assumed:
length. Date of predation failed to show a signiÞcant        t40 ⫽ ⫺5.00; P ⬍ 0.001). The statistical signiÞcance of
effect, with female pronotum length showing a positive       this comparison did not change when the cannibalized
relationship with prey length (generalized linear model:     males were included in analysis (LeveneÕs test, nor-
likelihood ratio ␹2 ⫽ 8.0; whole-model P ⬍ 0.05; prono-      mality of data not assumed: t46 ⫽ ⫺2.78; P ⬍ 0.01).
tum P ⬍ 0.01; date P ⬎ 0.9). Similar results were obtained      Over all years, we measured the rate of abdominal
when conspeciÞc males were included in analysis (gen-        expansion for 50 young adult females. Pronotum
eralized linear model: likelihood ratio ␹2 ⫽ 6.9; whole-     length did not affect the rate of abdominal expansion,
model P ⬍ 0.05; pronotum P ⬍ 0.01; date P ⬎ 0.5).            but date of Þrst measurement had a signiÞcant effect,
February 2014                  MAXWELL AND FRINCHABOY: INTRASPECIFIC SIZE VARIATION IN S. limbata                            97

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   Fig. 4. Date of Þrst measurement of dorsoventral abdominal girth (millimeters) for newly emerged adult females in the
Þeld and subsequent rate of abdominal expansion (millimeters per day ), 2008Ð2011. Numerical dates are Julian dates, where
1 August ⫽ 213. Crosses: 2008; black circles: 2009; triangles: 2010; white circles: 2011. Possible outliers are indicated by the
letters A, B, and C.

with females maturing later in the season showing                   Female Fecundity and Ootheca Mass. For female fe-
greater rates of expansion (Fig. 4; ANCOVA: F5,44 ⫽              cundity (2006 and 2008), egg number increased with
3.14; whole-model P ⬍ 0.05; date P ⬍ 0.001; pronotum             pronotum length (Fig. 6a; Multiple regression: F2,27 ⫽
P ⬎ 0.2; year P ⬎ 0.1). Exclusion of three outliers (A,          8.5; adjusted R2 ⫽ 0.34; whole-model P ⬍ 0.001; pro-
B, and C) reduced the statistical signiÞcance of the             notum length P ⬍ 0.01; year P ⬎ 0.7). For the mass of
overall ANCOVA model, but the signiÞcance of the                 the Þrst ootheca (2010), ootheca mass increased with
three variables did not change (ANCOVA: F5,41 ⫽                  both pronotum length and body condition (Fig. 6b;
2.32; whole-model P ⫽ 0.061; date P ⬍ 0.01; pronotum             Stepwise multiple regression: F2,23 ⫽ 16.8; adjusted
P ⬎ 0.3; year P ⬎ 0.2).                                          R2 ⫽ 0.56; whole-model P ⬍ 0.001; pronotum length
   Reproduction: Male Attraction, Natural Pairings,              P ⬍ 0.001; body condition index ratio P ⬍ 0.01). We
Fecundity, and Ootheca Mass. Field Experiment: Fe-               obtained statistically equivalent results when using
male Length and Male Attraction. In total, we found 56
males on the femalesÕ cages. We did not Þnd any males
on the six empty control cages, so we excluded these
empty cages from analysis. The average number of
males per female was similar for short females
(mean ⫾ SE ⫽ 2.6 ⫾ 0.9 males; n ⫽ 12) and long
females (mean ⫾ SE ⫽ 2.1 ⫾ 0.8 males, n ⫽ 12; t-test:
t22 ⫽ 0.4, P ⬎ 0.6). To examine possible nonindepen-
dence of arriving males, we analyzed male arrivals as
presence-absence data (i.e., presence ⫽ one or more
males per check). The 56 males can be regarded as 33
independent occurrences; that is, exactly one male
was found on 22 checks, with two or more males found
on 11 checks. For these presence-absence data, the
average number of occurrences of at least one male
was similar for short females (mean ⫾ SE ⫽ 1.6 ⫾ 0.3
occurrences; n ⫽ 12) and long females (mean ⫾ SE ⫽
1.2 ⫾ 0.4 occurrences, n ⫽ 12; t-test: t22 ⫽ 0.9, P ⬎ 0.3).
   Field Observations: Female and Male Pairings. For
natural pairings in the Þeld, paired females tended to
be longer than unpaired females, but this difference
                                                                   Fig. 5. Pronotum length (millimeters) of females in
was not statistically signiÞcant in any year (Fig. 5). For       natural pairings in Þeld, 2008Ð2011. Mean ⫾ SE plotted.
a given year, sample sizes were 9 Ð36 paired females             White diamonds: unpaired females (n ⫽ 71Ð178 per year).
and 71Ð178 unpaired females. For the combined years              Black diamonds: paired females (n ⫽ 9Ð36 per year). Un-
2009 Ð2011, adult age was known for 20 of the paired             paired t-tests compare pronotum length of unpaired and
females (mean ⫾ SE ⫽ 15 ⫾ 2 d; range ⫽ 4 Ð28 d).                 paired females within each year; NS: P ⬎ 0.05.
98                                     ENVIRONMENTAL ENTOMOLOGY                                             Vol. 43, no. 1

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   Fig. 6. Female pronotum length (millimeters) and measures of reproduction. (a) Fecundity (number of mature eggs
in body at death). White circles: 2006 (n ⫽ 18). Black circles: 2008 (n ⫽ 12). (b) Mass of Þrst ootheca (g), 2010 (n ⫽ 26).

regression residuals as the measure of female body             more successful in subduing longer prey. Recent work
condition. The average interval from copulation to             on mantids in captivity has begun to address this ques-
Þrst ootheca was 12 d (SE ⫽ 2 d; n ⫽ 26).                      tion but from different perspectives. In the mantid T.
                                                               aridifolia, Whitman and Vincent (2008) reported a
                                                               positive correlation between prey size and adult man-
                                                               tid mass, combining attacks by males and the larger
   The current study reveals several consequences of           females. However, recent interspeciÞc comparisons of
intraspeciÞc variation in body size, particularly with         mantid species in captivity indicate that target sizes
respect to prey size, prey breadth, female fecundity,          that elicit strike behaviors are not related to predator
and ootheca mass. Longer females were found with               species size (Prete et al. 2011, 2013). Clearly, more
longer prey in the Þeld, as well as greater breadth of         experimental work on the effects of predator size on
prey size, than shorter females. These results are in          attack rates and capture success is warranted, with
agreement with empirical studies on intraspeciÞc vari-         attention to interspeciÞc and intraspeciÞc variation.
ation in predator size, prey size, and diet breadth in            One form of predation, intraspeciÞc predation
many taxa, including insects (Schoener 1971, Wilson            (cannibalism), was observed in the current study, in
1975, Cohen et al. 1993, Costa 2009), as well as Hol-          two contexts: intersexual and intrasexual. With regard
lingÕs predictions developed for mantids based on              to intersexual cannibalism, females that were ob-
foreleg morphology (Holling 1964, Holling et al.               served to cannibalize males in the Þeld were of similar
1976). In the current study, we note that it is difÞcult       length to noncannibalistic females. This result aligns
to ascertain whether longer females were more likely           with captive work on S. limbata and P. albofimbriata
to strike at longer prey, or whether strike rates were         (Barry et al. 2008, Barry 2010, Maxwell et al. 2010b).
constant across female sizes and longer females were           In these studies, poorly fed females were more likely
February 2014               MAXWELL AND FRINCHABOY: INTRASPECIFIC SIZE VARIATION IN S. limbata                   99

to cannibalize males than were well-fed females, while     feeding regime has been manipulated, with female
neither female pronotum length nor male pronotum           length being standardized or left unexamined (e.g.,
length inßuenced the occurrence of cannibalism. Fur-       Lelito and Brown 2006, 2008; Maxwell et al. 2010a,b;
thermore, Maxwell et al. (2010b) failed to determine       Barry 2010; Barry et al. 2010). Therefore, it is difÞcult
that the degree of length dimorphism between paired        to draw generalizations about the importance of
females and males inßuenced the occurrence of can-         female length on male behavior at this stage. Further-
nibalism. However, it may be premature to conclude         more, research on cannibalistic arachnids reveals male
that female length does not inßuence the occurrence        preferences for large females (Prenter et al. 1994,
of cannibalism in mantids. In spiders, varied results      Hoeßer 2007), with at least one species preferring
have been reported, with many species showing a            small females (Moya-Laraño et al. 2003). Thus, female
positive relationship between mate size dimorphism         length, in addition to female feeding regime, merits
and cannibalism, whereas others show no, or even a         more consideration in studies of mantid mating be-
negative, relationship (reviewed in Wilder and Ryp-        havior.
stra 2008). Female hunger also plays an important role        In the current study, our expectations were con-

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in the occurrence of cannibalism in some spiders,          Þrmed regarding female length and measures of egg
whereas other spider species show little effect of fe-     production, with longer females having higher fecun-
male hunger (reviewed in Wilder et al. 2009). Given        dity and laying heavier oothecae. These results are
this range of results across spider species, more con-     consistent with the many empirical studies that dem-
sideration of absolute length and sexual size dimor-       onstrate that female fecundity increases with body
phism is needed in studies of mating behavior and          size within insect species (Honek̆ 1993, Whitman
cannibalism in mantids.                                    2008) and other taxa (Peters 1983, Roff 1992). In
   Intrasexual cannibalism, speciÞcally cannibalism        insects, it is reasonable to assume that female abdom-
among adult females, was observed in the current           inal length increases with body length or pronotum
study, which is consistent with previous observations      length, thereby enabling longer females to hold more
in the Þeld for S. limbata and other mantids (Hurd et      eggs. Preziosi et al. (1996) directly tested this assump-
al. 1994, Maxwell and Eitan 1998). This form of can-       tion in the water strider Aquarius remigis Say, dem-
nibalism might reßect overall food limitation in the       onstrating that larger females showed higher fecun-
Þeld or individual variation in foraging success (Fagan
                                                           dities because they had larger abdomens. Other
and Hurd 1991). Alternatively, interfemale cannibal-
                                                           authors indicate that larger abdomens may also pro-
ism might be a manifestation of interference compe-
                                                           vide increased space for accessory materials or organs
tition over ambush sites, or possibly over sites for
                                                           involved in egg production and oviposition (Wickman
“calling” (pheromone emission) and oviposition. If
                                                           and Karlsson 1989, Roff 1992). This consideration is
such interference competition is occurring, then lon-
                                                           especially relevant for mantids, which lay eggs in ooth-
ger females are likely to overpower and consume
shorter females (Fox 1975, Polis 1981), similar to how     ecae, requiring the production and storage of the en-
size difference between mantid nymphs reliably dif-        veloping spume material. In mantids, longer females
ferentiates the cannibal from the victim (Hurd 1988).      may have greater abdominal space for more eggs as
Although observations of femaleÐfemale cannibalism         well as more oothecal spume.
in the current study were too few to do a rigorous            In addition to increased fecundity and ootheca
analysis of the effect of relative length, we note that    mass, longer females may have longer reproductive
the cannibal female was longer than the victim female      life spans in nature. In the current study, longer fe-
in the two cases where relative lengths were known.        males consistently matured earlier in the season, as
The possibility of cannibalism in the context of inter-    seen in the strong negative relationship between date
female competition deserves further investigation          of adult emergence and female pronotum length in all
(Polis 1981, Maxwell 1999).                                years. These early emergence dates are expected to
   Regarding female length and male attraction, we         contribute to longer reproductive life spans for longer
held no a priori expectations regarding the effect of      females. Early-maturing females, however, appear to
female length, as males may prefer longer females for      emerge during a more food-limited part of the season,
increased fecundity, or shorter females for reduced        as feeding rates in nature (measured by rates of ab-
risk of cannibalism (Bonduriansky 2001, Wilder and         dominal expansion) were higher later in the season.
Rypstra 2008). Our experimental and observational          Although smaller, later-emerging females might have
results on mating behavior fail to reveal an effect of     less time available for feeding, mating, and egg-laying,
female length. In the Þeld experiment on male attrac-      they might be reproductively active during a more
tion, longer females did not attract more males than       food-abundant part of the season. Late-season emer-
shorter females did. Given that the females were ob-       gence at small size, then, may involve the beneÞt of
scured with cotton gauze, it could be argued that this     increased prey abundance. While this might be a for-
result suggests that pheromone emission was not af-        tunate ecological coincidence in this study system,
fected by female length, but the males might still favor   small size can confer several additional advantages, as
longer or shorter females once they make visual con-       many empirical studies demonstrate that small size
tact. The natural pairings in the Þeld, however, fail to   can be less costly in terms of energetic and metabolic
indicate a length preference expressed by males. In        demands, movement costs, and susceptibility to water
studies of male mating behavior in mantids, female         and heat loss (Peters 1983, Hone and Benton 2005).
100                                       ENVIRONMENTAL ENTOMOLOGY                                               Vol. 43, no. 1

   The current study points to several ecological con-             Dussé, K., and L. E. Hurd. 1997. Food limitation reduces
sequences of large adult female size in the mantid S.                 body length in mantid nymphs, Tenodera sinensis Sau-
limbata, particularly larger prey size, broader diet, and             ssure (Mantodea: Mantidae): implications for Þtness.
increased egg production. While longer females may                    Proc. Entomol. Soc. Wash. 99: 490 Ð 493.
have longer reproductive life spans in nature, shorter             Ehrmann, R. 2002. Mantodea: Gottesanbeterinnen der
                                                                      Welt. Natur und Tier, Münster, Germany.
later-emerging females may reap the ecological ben-
                                                                   Fagan, W. F., and L. E. Hurd. 1991. Late season food level,
eÞt of feeding at higher rates as adults. Furthermore,                cannibalism, and oviposition in adult mantids (Or-
shorter females were not necessarily at a disadvantage                thoptera: Mantidae): sources of variability in a Þeld ex-
in attracting males. Thus, while larger adult size ap-                periment. Proc. Entomol. Soc. Wash. 93: 956 Ð961.
pears to provide several Þtness beneÞts, large size                Fagan, W. F., and L. E. Hurd. 1994. Hatch density variation
might not effect other Þtness components, or might                    of a generalist arthropod predator: population conse-
entail hidden costs.                                                  quences and community impact. Ecology 75: 2022Ð2032.
                                                                   Fagan, W. F., M. D. Moran, J. J. Rango, and L. E. Hurd. 2002.
                                                                      Community effects of praying mantids: a meta-analysis of

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                    Acknowledgments                                   the inßuences of species identity and experimental de-
                                                                      sign. Ecol. Entomol. 27: 385Ð395.
   We thank Goggy Davidowitz, Larry Hurd, Chad Johnson,            Fox, L. R. 1975. Cannibalism in naturalism populations.
Doug Whitman, and anonymous reviewers for constructive                Annu. Rev. Ecol. Syst. 6: 87Ð106.
comments. Our gratitude extends to the following for assis-        Hoefler, C. D. 2007. Male mate choice and size-assortative
tance in the Þeld: Kevin Gallego, Ted Maxwell, Jamie Mer-             pairing in a jumping spider, Phidippus clarus. Anim. Be-
edith, Scott Seyfried, Nate Seyfried, and Beth Sullivan. We           hav. 73: 943Ð954.
additionally thank the staff of the Owens Valley Laboratory        Holling, C. S. 1964. The analysis of complex population pro-
(University of California, White Mountain Research Station)           cesses. Canad. Entomol. 96: 335Ð347.
for accommodations and logistical support. National Univer-        Holling, C. S., R. L. Dunbrack, and L. M. Dill. 1976. Pred-
sity provided funding for this research. This research con-           ator size and prey size: presumed relationship in the
forms to the institutional requirements of National Univer-           mantid Hierodula coarctata Saussure. Canad. J. Zool. 54:
sity.                                                                 1760 Ð1764.
                                                                   Hone, D.W.E., and M. J. Benton. 2005. The evolution of
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   dom.                                                            Received 28 October 2012; accepted 20 October 2013.
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